Plant-mycorrhizal Interactions Research Articles

Ectomycorrhizal fungi enhance pine growth by stimulating iron-dependent mechanisms with trade-offs in symbiotic performance.

Iron (Fe) is crucial for metabolic functions of living organisms. Plants access occluded Fe through interactions with rhizosphere microorganisms and symbionts. Yet, the interplay between Fe addition and plant-mycorrhizal interactions, especially the molecular mechanisms underlying mycorrhiza-assisted Fe processing in plants, remains largely unexplored. We conducted mesocosms in Pinus plants inoculated with different ectomycorrhizal fungi (EMF) Suillus species under conditions with and without Fe coatings. Meta-transcriptomic, biogeochemical, and X-ray fluorescence imaging analyses were applied to investigate early-stage mycorrhizal roots. While Fe addition promoted Pinus growth, it concurrently reduced mycorrhiza formation rate, symbiosis-related metabolites in plant roots, and aboveground plant carbon and macronutrient content. This suggested potential trade-offs between Fe-enhanced plant growth and symbiotic performance. However, the extent of this trade-off may depend on interactions between host plants and EMF species. Interestingly, dual EMF species were more effective at facilitating plant Fe uptake by inducing diverse Fe-related functions than single-EMF species. This subsequently triggered various Fe-dependent physiological and biochemical processes in Pinus roots, significantly contributing to Pinus growth. However, this resulted in a greater carbon allocation to roots, relatively reducing the aboveground plant carbon content. Our study offers critical insights into how EMF communities rebalance benefits of Fe-induced effects on symbiotic partners.

Dueling Plant Phosphorus Acquisition Strategies Over a Geochemical Gradient: A Biogeochemistry Experiment Approach

Plants are likely to be phosphorus (P)-limited because of low availability of P to roots or mycorrhizae due to slow diffusion and high sorption in soils. Phosphorus sub-cycles (inorganic versus organic) also tend to vary predictably over gradients (Fig. 1A,B). Plant responses to mycorrhizal fungi also vary by plant species and grassland type (Reinhart et al. 2017). Mycorrhizae can scavenge nutrients (i.e. orthophosphate, organic-P); however, if they cannot solubilize calcium bound P, then geochemical gradients may constrain plant-mycorrhizal interactions (Fig. 1C). Calcareous soils are found in >30% of soils and are common in arid, semiarid, and semi-humid systems (e.g. grasslands, shrublands). We used geochemical and biogeochemical experiments to test hypotheses on P limitation and acquisition (Lajtha and Schlesinger 1988). Hypothesis: an increase in soil calcium carbonate (CaCO3) will 1) reduce soil P bioavailability (geochemical exp.), 2) reduce plant biomass and phosphorus uptake (biogeochemical exp.), and 3) shift P acquisition strategies (i.e. root mining, mycorrhizal scavenging) (biogeochemical exp., Fig. 1C). Experiments had a replacement series (CaCO3 to silica sand) geochemical treatment (CaCO3 additions: 0, 0.02, 0.10, and 0.30 [g × 100 g-1]) to simulate soil properties over natural grassland gradients. The biogeochemistry experiment was a completely randomized design with the geochemical and mycorrhizal fungi treatments (+, -) (4 × 2 factorial), 8 plant species, and 8 replications. Geochemical exp.’s response variables were soil extractable nutrients and pH. Biogeochemistry exp.’s response variables were nutrient uptake and plant performance. The geochemical experiment confirmed that increasing CaCO3 increased pHwater of subsurface soil (7.6 to 8.5), reduced the intensity of available P (assessed by anion exchange membranes) in treated soils by as much as 57%, and had no obvious effect on accessible P (Olsen-P). In other words, metaphorical cups of P (with straws) had similar amounts of accessible P per cup; however, additions of CaCO3 effectively reduced the straws’ diameter and limited (re-)supply of available P. On average, large additions of CaCO3 reduced plant biomass by 20% and plant uptake of P by 15% for the biogeochemistry experiment. On average, mycorrhizal fungi increased plant biomass by 6%. Rarely did mycorrhizal fungi and geochemical treatments interact and affect plant biomass. When they did interact, mycorrhizae benefited plants in pots with greater levels of P intensity (i.e. no or little added CaCO3) thereby suggesting mycorrhizae may not help to solubilize calcium bound P. These findings confirm CaCO3 in subsoils reduced the intensity of bioavailable P, which consequently decreased plant biomass and P uptake. However, we cannot rule out that CaCO3 additions may have additionally impacted plants response due to changes in micronutrient solubility (i.e. zinc), etc. (Lajtha and Schlesinger 1988). While plants tended to benefit from mycorrhizae, we found no evidence to support a prediction of the nutritional mutualisms hypothesis—that benefits are greatest under P-limitation. On the contrary, our data suggest that plants will rely more on root mining P acquisition strategies than mycorrhizal scavenging (Albornoz et al. 2020) where the inorganic-P sub-cycle dominates and P solubility is limited due to calcium-phosphate formation (Fig. 1C).

Epigenetic control is involved in molecular dialogue in plant-microbe symbiosis.

This article is a Commentary on Vigneaud et al. (2023), 238: 2561–2577.

Common and lifestyle‐specific traits of mycorrhizal root metabolome reflect ecological strategies of plant–mycorrhizal interactions

Abstract Mycorrhizas are widespread below‐ground symbioses formed between plant roots and soil fungi. This plant–fungal partnership impacts terrestrial ecosystems by mediating plant performance and biogeochemical processes. The influence of mycorrhizas on plant and ecosystem functioning is ultimately driven by the biological processes that regulate plant–mycorrhizal interactions. Although convergent patterns in morphological and genetic traits of mycorrhizas have been well‐documented and reflect key selection forces that shape the biology of mycorrhizas, generalizable traits of mycorrhizal‐associated root metabolome, which are more intimately linked to plant and ecosystem functioning, remain unexplored. Here, we compared mycorrhizal‐associated metabolome alterations across multiple plant–mycorrhizal fungus combinations. Specifically, we inoculated a phylogenetically diverse set of temperate tree species with either arbuscular mycorrhizal or ectomycorrhizal fungi (the two major mycorrhizal lifestyles). Using comprehensive metabolomics approaches, we then assessed the metabolome in mycorrhizal and non‐mycorrhizal roots and the corresponding leaves. Comparing across multiple plant–mycorrhizal fungus combinations, our data revealed metabolite alterations unique to mycorrhizal lifestyle as well as those common across plant–fungus combinations irrespective of lifestyles. Roots colonized by arbuscular mycorrhizal and ectomycorrhizal fungi accumulated different sets of carbohydrates, reflecting unique carbon allocation strategies for mycorrhizas. Arbuscular mycorrhizal roots accumulated cyclic polyols (e.g. inositols) inaccessible to their fungal partners, suggesting tight regulation of carbon partitioning. Such accumulation did not occur in ectomycorrhizal‐colonized roots, which instead accrued acyclic polyols (e.g. mannitol and arabitol) that were undetected in non‐mycorrhizal roots and likely of fungal origin. Mycorrhizas also altered specialized metabolism, featuring frequent increases in flavan‐3‐ols (e.g. catechins, gallocatechins, and their oligomers) but decreases in flavanols irrespective of mycorrhizal lifestyles, suggesting tactical reconfiguration of specialized metabolites to both facilitate and restrain the symbiont. These characteristic metabolite alterations were largely root specific and were not mirrored in leaves. Synthesis. Using multiple plant–mycorrhizal systems and metabolomics approaches, our study demonstrates that part of the metabolite alterations occurring during root–mycorrhizal interactions were relatively common across plant–mycorrhizal systems, with implications for both carbon partitioning and tissue protection strategies important for successful symbiosis. These generalizable patterns appear robust to the phylogenetic history of host plants and thus may be widespread in land plants.

Evidence for the evolution of native plant response to mycorrhizal fungi in post-agricultural grasslands.

Plant–microbe interactions play an important role in structuring plant communities. Arbuscular mycorrhizal fungi (AMF) are particularly important. Nonetheless, increasing anthropogenic disturbance will lead to novel plant–AMF interactions, altering longstanding co‐evolutionary trajectories between plants and their associated AMF. Although emerging work shows that plant–AMF response can evolve over relatively short time scales due to anthropogenic change, little work has evaluated how plant AMF response specificity may evolve due to novel plant–mycorrhizal interactions. Here, we examine changes in plant–AMF interactions in novel grassland systems by comparing the mycorrhizal response of plant populations from unplowed native prairies with populations from post‐agricultural grasslands to inoculation with both native prairie AMF and non‐native novel AMF. Across four plant species, we find support for evolution of differential responses to mycorrhizal inocula types, that is, mycorrhizal response specificity, consistent with expectations of local adaptation, with plants from native populations responding most to native AMF and plants from post‐agricultural populations responding most to non‐native AMF. We also find evidence of evolution of mycorrhizal response in two of the four plant species, as overall responsiveness to AMF changed from native to post‐agricultural populations. Finally, across all four plant species, roots from native prairie populations had lower levels of mycorrhizal colonization than those of post‐agricultural populations. Our results report on one of the first multispecies assessment of local adaptation to AMF. The consistency of the responses in our experiment among four species provides evidence that anthropogenic disturbance may have unintended impacts on native plant species' association with AMF, causing evolutionary change in the benefit native plant species gain from native symbioses.

Ectomycorrhizal access to organic nitrogen mediates CO2 fertilization response in a dominant temperate tree

Plant–mycorrhizal interactions mediate plant nitrogen (N) limitation and can inform model projections of the duration and strength of the effect of increasing CO2 on plant growth. We present dendrochronological evidence of a positive, but context-dependent fertilization response of Quercus rubra L. to increasing ambient CO2 (iCO2) along a natural soil nutrient gradient in a mature temperate forest. We investigated this heterogeneous response by linking metagenomic measurements of ectomycorrhizal (ECM) fungal N-foraging traits and dendrochronological models of plant uptake of inorganic N and N bound in soil organic matter (N-SOM). N-SOM putatively enhanced tree growth under conditions of low inorganic N availability, soil conditions where ECM fungal communities possessed greater genomic potential to decay SOM and obtain N-SOM. These trees were fertilized by 38 years of iCO2. In contrast, trees occupying inorganic N rich soils hosted ECM fungal communities with reduced SOM decay capacity and exhibited neutral growth responses to iCO2. This study elucidates how the distribution of N-foraging traits among ECM fungal communities govern tree access to N-SOM and subsequent growth responses to iCO2.

Influences of plant interspecific competition and arbuscular mycorrhizal fungi on nitrogen form preference of an invasive plant

Invasive plant species are often able to alter soils in a way that benefits their own fitness over that of native species. While interspecific competitions may drive species to acquire different forms of nitrogen (N) to avoid intensive competition, plant-mycorrhizal interactions can also influence plant nutrient acquisition. Yet, it is unclear whether a variation in N acquisition by an invasive species is driven by interspecific resource partitioning due to competition with native species or by its symbiosis with arbuscular mycorrhizal (AM) fungi. We conducted a pot experiment to examine the effects of competition and fungicide on the uptake of different N forms by Flaveria bidentis, an invasive plant having symbiotic relationships with AM fungi, and two coexisting native species, mycotrophic Bidens maximowicziana and non-mycotrophic Amaranthus retroflexus (referred to by genus hereafter), by growing them either in two-species mixtures or in monocultures. We found that the growth of Flaveria was suppressed by its association with AM fungi regardless of the presence of competing native species, but the degree of suppression was related to the native species with which Flaveria competed. When growing in monocultures, all three species showed a strong preference for NO3−-N over NH4+-N and glycine-N regardless of mycorrhizal status. However, under competition conditions, Flaveria increased 15N recovery in any form of N available (in particular NH4+-15N), depending on neighboring plant identity and AM fungi association, whereas Amaranthus specially tended to decrease NH4+-15N uptake when competing with Flaveria, suggesting a niche complementarity in the utilization of N between two species. Our findings suggested that AM fungi may have the potential to limit the invasion of Flaveria, in the short term, and that interspecific competition plays an important role in partitioning soil N acquisition between plant species.

Mediation of plant-mycorrhizal interaction by a lectin receptor-like kinase.

The molecular mechanisms underlying mycorrhizal symbioses, the most ubiquitous and impactful mutualistic plant-microbial interaction in nature, are largely unknown. Through genetic mapping, resequencing and molecular validation, we demonstrate that a G-type lectin receptor-like kinase (lecRLK) mediates the symbiotic interaction between Populus and the ectomycorrhizal fungus Laccaria bicolor. This finding uncovers an important molecular step in the establishment of symbiotic plant-fungal associations and provides a molecular target for engineering beneficial mycorrhizal relationships.

Cooperation and coexpression: How coexpression networks shift in response to multiple mutualists.

A mechanistic understanding of community ecology requires tackling the nonadditive effects of multispecies interactions, a challenge that necessitates integration of ecological and molecular complexity-namely moving beyond pairwise ecological interaction studies and the "gene at a time" approach to mechanism. Here, we investigate the consequences of multispecies mutualisms for the structure and function of genomewide differential coexpression networks for the first time, using the tractable and ecologically important interaction between legume Medicago truncatula, rhizobia and mycorrhizal fungi. First, we found that genes whose expression is affected nonadditively by multiple mutualists are more highly connected in gene networks than expected by chance and had 94% greater network centrality than genes showing additive effects, suggesting that nonadditive genes may be key players in the widespread transcriptomic responses to multispecies symbioses. Second, multispecies mutualisms substantially changed coexpression network structure of 18 modules of host plant genes and 22 modules of the fungal symbionts' genes, indicating that third-party mutualists can cause significant rewiring of plant and fungal molecular networks. Third, we found that 60% of the coexpressed gene sets that explained variation in plant performance had coexpression structures that were altered by interactive effects of rhizobia and fungi. Finally, an "across-symbiosis" approach identified sets of plant and mycorrhizal genes whose coexpression structure was unique to the multiple mutualist context and suggested coupled responses across the plant-mycorrhizal interaction to rhizobial mutualists. Taken together, these results show multispecies mutualisms have substantial effects on the molecular interactions in host plants, microbes and across symbiotic boundaries.

Plant-mycorrhizal interactions mediate plant community coexistence by altering resource demand.

As the diversity of plants increases in an ecosystem, so does resource competition for soil nutrients, a process that mycorrhizal fungi can mediate. The influence of mycorrhizal fungi on plant biodiversity likely depends on the strength of the symbiosis between the plant and fungi, the differential plant growth responses to mycorrhizal inoculation, and the transfer rate of nutrients from the fungus to plant. However, our current understanding of how nutrient-plant-mycorrhizal interactions influence plant coexistence is conceptual and thus lacks a unified quantitative framework. To quantify the conditions of plant coexistence mediated by mycorrhizal fungi, we developed a mechanistic resource competition model that explicitly included plant-mycorrhizal symbioses. We found that plant-mycorrhizal interactions shape plant coexistence patterns by creating a tradeoff in resource competition. Especially, a tradeoff in resource competition was caused by differential payback in the carbon resources that plants invested in the fungal symbiosis and/or by the stoichiometric constraints on plants that required additional, less-beneficial, resources to sustain growth. Our results suggested that resource availability and the variation in plant-mycorrhizal interactions act in concert to drive plant coexistence patterns. Applying our framework, future empirical studies should investigate plant-mycorrhizal interactions under multiple levels of resource availability.

Relationship between plant growth and organic acid exudates from ectomycorrhizal and non-ectomycorrhizal Pinus patula

Plant–mycorrhizal interaction is an important association in the ecosystem with significant impacts on the physical, biological and chemical properties of the soil. In the present study, potential relationships that exist between organic acid production by ectomycorrhizal pine seedlings and plant parameters in the absence of any significant environmental stress were investigated. The aim of the study was to investigate the contribution of organic acid production to plant growth. Four different ectomycorrhizal fungi were used in a mycorrhizal synthesis experiment to colonise roots of Pinus patula. Ectomycorrhizal and non-ectomycorrhizal plants were used in a pot trial experiment that lasted for 24 weeks. After harvesting, plant materials as well as soil samples underwent different analyses, which included the determination of pH, organic acids, plant biomass, and foliar and root phosphorus and potassium. The results indicated a significant interaction (P<0.0001) between fungal type and organic acid production. This reflects the influence of fungal type on organic acid production. However, it was observed that organic acids secreted into the soil are not directly linked with the quantity of nutrients detected in either the root or shoot, but seemed to positively influence plant growth as reflected in the result from root and shoot biomass.

Resource availability and imbalance affect plant–mycorrhizal interactions: a field test of three hypotheses

Ecological stoichiometry can explain major trends in how interactions among species change across fertility gradients, but important questions remain. For example, stoichiometry predicts that fertilization should cause plants to reduce carbon allocation to arbuscular mycorrhizal fungi and, consequently, reduce fungal abundance, but responses in the field are highly variable. In a field experiment, we tested three hypotheses that could drive this variation: (1) fungi are nitrogen limited in very nitrogen-poor soils, so fertilization increases their abundance; (2) the N:P ratio of fertilization affects plant carbon allocation to fungi; (3) plant species differences affect fungal response. Our results support all three hypotheses: stoichiometry and species idiosyncrasies jointly determined fungal response to fertilization. We provide field evidence in support of the hypothesis that nitrogen can limit fungal abundance in temperate grasslands. We also show that fungal abundance in soil (hyphal length) differed beneath two dominant plant species: big bluestem (Andropogon gerardii) and smooth brome (Bromus inermis). These grass species also differed in the degree to which they reduced root colonization with fertilization, but these differences in allocation did not lead to differential responses to fertilization in terms of fungal abundance in the soil. This study shows that, while ecological stoichiometry is a useful framework for understanding the effects of eutrophication on this important and widespread species interaction, including these subtleties can increase the predictive power of the theory.

Asociación simbiótica entre hongos micorrízicos arbusculares y el sistema radicular de plántulas de cacao (Theobroma cacao L.): efecto de la formononetina y la disponibilidad de fósforo en el suelo.

La simbiosis entre plantas de cacao y hongos micorrízicos arbusculares (HFMA) confiere beneficios nutricionales y competitivos a la planta, especialmente en condiciones de baja disponibilidad de nutrientes. Se evaluó tres niveles de fósforo (5, 20 y 40 ppm) y la presencia o ausencia de isoflavonoide formononetina. El nivel 14 ppm de P sin el isoflavonoide fue el tratamiento testigo. Todos los tratamientos fueron inoculados con HFMA a excepción del tratamiento control. Se utilizó un diseño completamente al azar y se determinaron caracteres morfológicos de la planta a los 70, 110 y 150 días después de la inoculación. Los resultados no mostraron respuesta diferencial a los caracteres morfológicos de la planta por la disponibilidad del isoflavonoide durante los tres muestreos. La longitud radicular presentó diferencias significativas en los muestreo (70, 110 y 150 días de inoculación), siendo esta respuesta dependiente de la disponibilidad de P y la interacción plantamicorriza. El número de esporas mostró diferencias entre los muestreos de 110 y 150 días de inoculación en presencia y ausencia del isoflavonoide, sugiriendo una rápida estimulación en el establecimiento de la relación simbiótica por la formononetina en el proceso de germinación y formación de estructuras fúngicas.

Interactions of biotic and abiotic environmental factors in an ectomycorrhizal symbiosis, and the potential for selection mosaics.

BackgroundGeographic selection mosaics, in which species exert different evolutionary impacts on each other in different environments, may drive diversification in coevolving species. We studied the potential for geographic selection mosaics in plant-mycorrhizal interactions by testing whether the interaction between bishop pine (Pinus muricata D. Don) and one of its common ectomycorrhizal fungi (Rhizopogon occidentalis Zeller and Dodge) varies in outcome, when different combinations of plant and fungal genotypes are tested under a range of different abiotic and biotic conditions.ResultsWe used a 2 × 2 × 2 × 2 factorial experiment to test the main and interactive effects of plant lineage (two maternal seed families), fungal lineage (two spore collections), soil type (lab mix or field soil), and non-mycorrhizal microbes (with or without) on the performance of plants and fungi. Ecological outcomes, as assessed by plant and fungal performance, varied widely across experimental environments, including interactions between plant or fungal lineages and soil environmental factors.ConclusionThese results show the potential for selection mosaics in plant-mycorrhizal interactions, and indicate that these interactions are likely to coevolve in different ways in different environments, even when initially the genotypes of the interacting species are the same across all environments. Hence, selection mosaics may be equally as effective as genetic differences among populations in driving divergent coevolution among populations of interacting species.

Soil temperature affects carbon allocation within arbuscular mycorrhizal networks and carbon transport from plant to fungus

AbstractHow soil carbon balance will be affected by plant–mycorrhizal interactions under future climate scenarios remains a significant unknown in our ability to forecast ecosystem carbon storage and fluxes. We examined the effects of soil temperature (14, 20, 26 °C) on the structure and extent of a multispecies community of arbuscular mycorrhizal (AM) fungi associated with Plantago lanceolata. To isolate fungi from roots, we used a mesh‐divided pot system with separate hyphal compartments near and away from the plant. A 13C pulse label was then used to trace the flow of recently fixed photosynthate from plants into belowground pools and respiration. Temperature significantly altered the structure and allocation of the AM hyphal network, with a switch from more vesicles (storage) in cooled soils to more extensive extraradical hyphal networks (growth) in warmed soils. As soil temperature increased, we also observed an increase in the speed at which plant photosynthate was transferred to and respired by roots and AM fungi coupled with an increase in the amount of carbon respired per unit hyphal length. These differences were largely independent of plant size and rates of photosynthesis. In a warmer world, we would therefore expect more carbon losses to the atmosphere from AM fungal respiration, which are unlikely to be balanced by increased growth of AM fungal hyphae.

Geographic structure in a widespread plant–mycorrhizal interaction: pines and false truffles

Mutualistic interactions are likely to exhibit a strong geographic mosaic in their coevolutionary dynamics, but the structure of geographic variation in these interactions is much more poorly characterized than in host-parasite interactions. We used a cross-inoculation experiment to characterize the scales and patterns at which geographic structure has evolved in an interaction between three pine species and one ectomycorrhizal fungus species along the west coast of North America. We found substantial and contrasting patterns of geographic interaction structure for the plants and fungi. The fungi exhibited a clinal pattern of local adaptation to their host plants across the geographic range of three coastal pines. In contrast, plant growth parameters were unaffected by fungal variation, but varied among plant populations and species. Both plant and fungal performance measures varied strongly with latitude. This set of results indicates that in such widespread species interactions, interacting species may evolve asymmetrically in a geographic mosaic because of differing evolutionary responses to clinally varying biotic and abiotic factors.

Correlations between foliar δ15N and nitrogen concentrations may indicate plant-mycorrhizal interactions.

Nitrogen isotope measurements may provide insights into changing interactions among plants, mycorrhizal fungi, and soil processes across environmental gradients. Here, we report changes in δ15N signatures due to shifts in species composition and nitrogen (N) dynamics. These changes were assessed by measuring fine root biomass, net N mineralization, and N concentrations and δ15N of foliage, fine roots, soil, and mineral N across six sites representing different post-deglaciation ages at Glacier Bay, Alaska. Foliar δ15N varied widely, between 0 and -2‰ for nitrogen-fixing species, between 0 and -7‰ for deciduous non-fixing species, and between 0 and -11‰ for coniferous species. Relatively constant δ15N values for ammonium and generally low levels of soil nitrate suggested that differences in ammonium or nitrate use were not important influences on plant δ15N differences among species at individual sites. In fact, the largest variation among plant δ15N values were observed at the youngest and oldest sites, where soil nitrate concentrations were low. Low mineral N concentrations and low N mineralization at these sites indicated low N availability. The most plausible mechanism to explain low δ15N values in plant foliage was a large isotopic fractionation during transfer of nitrogen from mycorrhizal fungi to plants. Except for N-fixing plants, the foliar δ15N signatures of individual species were generally lower at sites of low N availability, suggesting either an increased fraction of N obtained from mycorrhizal uptake (f), or a reduced proportion of mycorrhizal N transferred to vegetation (T r). Foliar and fine root nitrogen concentrations were also lower at these sites. Foliar N concentrations were significantly correlated with δ15N in foliage of Populus, Salix, Picea, and Tsuga heterophylla, and also in fine roots. The correlation between δ15N and N concentration may reflect strong underlying relationships among N availability, the relative allocation of carbon to mycorrhizal fungi, and shifts in either f or T r.